Hologenome theory of evolution
The hologenome theory of evolution[1][2][3][4] recasts the individual animal or plant (and other multicellular organisms) as a community or a "holobiont" – the host plus all of its symbiotic microbes.
Holobionts and hologenomes are structural entities[5] that replace misnomers in the context of host-microbiota symbioses such as superorganism (i.e., an integrated social unit composed of conspecifics), organ, and metagenome.
Although there is a rich literature on binary host–microbe symbioses, the hologenome concept distinguishes itself by including the vast symbiotic complexity inherent in many multicellular hosts.
Lynn Margulis coined the term holobiont in her 1991 book Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis (MIT Press),[6] though this was not in the context of diverse populations of microbes.
In his lecture, Jefferson argued that these were likely not contamination, but rather essential components of the samples that reflected the actual genetic composition of the organism being studied, integral to the complex system in which it lives.
Observations on the ubiquity of microbes in plant and soil samples as well as laboratory work on molecular genetics of vertebrate-associated microbial enzymes impacting hormone action informed this hypothesis.
[11] At the 14th South African Congress of Biochemistry and Molecular Biology in 1997,[12] Jefferson described how the modulation of steroid and other hormone levels by microbial glucuronidases and arylsulfatase profoundly impacted the performance of the composite entity.
In his lectures, Jefferson coined and defined the term 'Ecotherapeutics', referring to adjustment of the population structure of the microbial composition in plants and animals - the microbiome - and their support ecosystem to improve performance.
[2] In 2013, Robert Brucker and Seth Bordenstein[17] re-invigorated the hologenome concept by showing that the gut microbiomes of closely related Nasonia wasp species are distinguishable, and contribute to hybrid death.
Hormones mediate critical activities in vertebrates, including ontogeny, somatic and reproductive physiology, sexual development, performance and behaviour.
Thus the concentration and bioavailability of many of the hormones is impacted by microbial cleavage of conjugated intermediaries, itself determined by a diverse population with redundant enzymatic capabilities.
Studies by Froebe et al.[18] in 1990 indicating that essential mating pheromones, including androstenols, required activation by skin-associated microbial glucuronidases and sulfatases.
In the Mediterranean Sea, the bleaching of Oculina patagonica was first described in 1994 and, through a rigorous application of Koch's Postulates, determined to be due to infection by Vibrio shiloi.
By altering its microbial composition, the "holobiont" can adapt to changing environmental conditions far more rapidly than by genetic mutation and selection in the host species alone.
Extrapolating the coral probiotic hypothesis to other organisms, including higher plants and animals, led to the Rosenberg's support for and publications around the hologenome theory of evolution.
Corals also have a sexual mode of reproduction, resulting in planktonic larva; it is less clear whether microbial associations persist through this stage of growth.
A well-studied example is the nocturnally feeding squid Euprymna scolopes, which camouflages its outline against the moonlit ocean surface by emitting light from its underside with the aid of the symbiotic bacterium Vibrio fischeri.
For example, in the stink bug Nezara viridula, the vertical transmission rate of symbionts, which females provide to offspring by smearing the eggs with gastric caeca, was 100% at 20 °C, but decreased to 8% at 30 °C.
[citation needed] Lamarckism, the concept that an organism can pass on characteristics that it acquired during its lifetime to its offspring (also known as inheritance of acquired characteristics or soft inheritance) incorporated two common ideas of its time: Although Lamarckian theory was rejected by the neo-Darwinism of the modern evolutionary synthesis in which evolution occurs through random variations being subject to natural selection, the hologenome theory has aspects that harken back to Lamarckian concepts.
[34] The pea aphid Acyrthosiphon pisum maintains an obligate symbiotic relationship with the bacterium Buchnera aphidicola, which is transmitted maternally to the embryos that develop within the mother's ovarioles.
It has been suggested that the symbiotic bacteria changed the levels of cuticular hydrocarbon sex pheromones,[42] however several other research papers have been unable to replicate this effect.
[43][44][45] Zilber-Rosenberg and Rosenberg (2008) have tabulated many of the ways in which symbionts are transmitted and their contributions to the fitness of the holobiont, beginning with mitochondria found in all eukaryotes, chloroplast in plants, and then various associations described in specific systems.
The microbial contributions to host fitness included provision of specific amino acids, growth at high temperatures, provision of nutritional needs from cellulose, nitrogen metabolism, recognition signals, more efficient food utilization, protection of eggs and embryos against metabolism, camouflage against predators, photosynthesis, breakdown of complex polymers, stimulation of the immune system, angiogenesis, vitamin synthesis, fiber breakdown, fat storage, supply of minerals from the soil, supply of organics, acceleration of mineralization, carbon cycling, and salt tolerance.
The rigorous satisfaction of Koch's postulates, as employed in Kushmaro et al. (1997),[24] is generally accepted as providing a definitive identification of infectious disease agents.
Although the hologenome theory is still being debated, it has gained a significant degree of popularity within the scientific community as a way of explaining rapid adaptive changes that are difficult to accommodate within a traditional Darwinian framework.
Recently, Forest L Rohwer and colleagues developed a novel statistical test to examine the potential for the hologenome theory of evolution in coral species.
The authors conclude: "Identification of these two symbiont communities supports the holobiont model and calls into question the hologenome theory of evolution."
